Neonicotinoids alter food preferences and colony behaviour in bees

The relationship between neonicotinoid pesticides and pollinator decline
has been the subject of a variety of research studies in recent years.
These widely-used pesticides are thought to contribute to the observed
reduction in the populations of bees and other pollinators because they
are applied to areas where bees forage. Residues have been detected in
bee-collected pollen and experimental evidence has pointed to a
correlation between exposure and bee and colony fitness.

In a recent article Crall et al. showed that bees exposed to neonicotinoids spent less time nursing larvae, had an impaired ability to warm the nest and to build insulating wax caps around the colony (1). On 27th April 2018 the EU voted to extend the ban on the outdoor use of three neonicotinoids: Clothianidin, Imidacloprid and Thiamethoxam. These pesticides had already been banned in 2013 for oil seed rape and spring cereal seed treatments as well as winter cereal crop sprays. However, until April this year they could still be used for sugar beet, in winter cereal seed treatments and for horticultural uses. This latest sanction, unlike the 2013 ban, was supported by the UK government. This recent move by the EU follows a European Food Safety Authority report that found that neonicotinoids posed a threat to all species of bees no matter where or how the chemicals were used in an outdoor environment.

Figure 1. Buff Tailed Bee. Credit: Clare Topping

However, Thiacloprid and other neonicotinoids remain exempt and all these pesticides can still be used in greenhouses. Furthermore, on 11th October 2018, another neonicotinoid, Sequoia, was authorised in the UK for use in greenhouses. Despite protests from the farming community in 2013, in December 2017 Buglife reported higher crop yields across the EU since the initial ban (2)

A previous ECG Bulletin (3) covered a World Integrated Assessment (WIA) study on the possible detrimental effects on pollinator populations and the impacts on biodiversity and food security, whilst the February 2017 ECG Bulletin (4) featured interviews with Dr Ben Woodstock (CEH) and Prof Simon Potts (Reading University) giving their views on the role played by bumblebees in pollination and the impact of their decline on food security. This update reviews the results in a recently published paper by Arce et al. that looks at the risk that neonicotinoid pesticides are likely to pose to pollinators such as bumblebees (5).

Using Bombus terrestris, one of the UK’s six commonest bumblebees and one often bought for commercial crop pollination, as the subject, the authors examined the behaviour of colonies of these bees when exposed to varying levels of neonicotinoids in sucrose solutions. Ten separate colonies were given the option of 0, 2 and 11 ppb (parts per billion) Thiamethoxam in six different dispensers. For ten days they measured how often the bees visited each of the concentrations and how much solution they took. The authors also looked at the behaviour of individually tagged bees over the same time period. Many of the previously published trials only studied the impact of neonicotinoids on bees by feeding them with spiked food; the bees were not given an option of ‘no pesticide’ and therefore their ability to detect and avoid neonicotinoids was not assessed. The only previous study examining the preferences of bees when given a choice of sugar solution with or without neonicotinoids was conducted over a 24 hour period and showed that, whilst bees could not detect the tested pesticides through their proboscis, individual bees consumed more sucrose laced with pesticides than without (6). By continuing the study over ten days, Arce and co-workers hoped to assess the risk rather than the hazard to the bees, i.e. what the likelihood of their exposure would be as well as the likely consequence of exposure. By using colonies, rather than individual bees, the researchers hoped to ensure that they mimicked conditions in the wild by also allowing social cues to be passed between bees. A previous study using different coloured feeders (7) showed that as colonies gain experience they can adapt their behaviour to overcome innate behaviours such as colour preferences of flowers.

In this study, bees were initially attracted preferentially to either the 0 or the 11 ppb solution over the 2 ppb solution, with correspondingly more of the former solutions being consumed by the bees. Over time, however, the bees preferentially moved to the 2 ppb solution, with fewer visits to the 0 ppb solution. The proportion of visits to the higher concentration remained about the same. Part way through the study, the position of the solutions was randomly changed in case there were learned behaviours and preferences not related to the concentration of Thiamethoxam. However, the trend remained the same with the bees preferring the 2 ppb solution so it would appear that the foragers could detect the Thiamethoxam and change their behaviour accordingly. This preference increased at approximately 1% per day so that by day 10 there were 28% more visits to the 2 ppb feeders than to the 0 ppb feeders. The studies of tagged bees, which were classed as experienced foragers, also showed the same increasing rate of preference for the 2 ppb solution even though initially they showed a strong preference for the 0 ppb feeder indicating an initial aversion to the Thiamethoxam (42% of visits). As with a previous study by Baracchi et al. (7), this work indicates that the presence of a neonicotinoid gradient alters the attractiveness of the food to bees and that they seem to prefer lower concentrations. In the study by Baracchi et al., bumblebees were deterred by higher doses of neonicotinoids, but attracted to lower doses and more quickly learned to associate these spiked flower feeders with reward. It was suggested that there might be a therapeutic alkaloid within the neonicotinoid which the bees preferentially seek out at low concentrations. These alkaloids were also thought to act as a psychostimulant in invertebrates which excites their reward system and leads them to a preference for the neonicotinoid laced sucrose.

ConclusionsThe recent work of Arce et al. concludes that the risk that bees will be exposed to neonicotinoids is higher than initially thought from previous trials as the bees seem to develop a preference for these chemicals and potentially transmit this preference to the colony. As studies continue, it appears that the impact of these pesticides on bumblebees and potentially other pollinators is more far-reaching and complex than initially assumed.